Bottom Line:
Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history.These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

Background: The chaetognaths (arrow worms) have puzzled zoologists for years because of their astonishing morphological and developmental characteristics. Despite their deuterostome-like development, phylogenomic studies recently positioned the chaetognath phylum in protostomes, most likely in an early branching. This key phylogenetic position and the peculiar characteristics of chaetognaths prompted further investigation of their genomic features.

Results: Transcriptomic and genomic data were collected from the chaetognath Spadella cephaloptera through the sequencing of expressed sequence tags and genomic bacterial artificial chromosome clones. Transcript comparisons at various taxonomic scales emphasized the conservation of a core gene set and phylogenomic analysis confirmed the basal position of chaetognaths among protostomes. A detailed survey of transcript diversity and individual genotyping revealed a past genome duplication event in the chaetognath lineage, which was, surprisingly, followed by a high retention rate of duplicated genes. Moreover, striking genetic heterogeneity was detected within the sampled population at the nuclear and mitochondrial levels but cannot be explained by cryptic speciation. Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.

Conclusion: These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history. These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

Figure 8: Categories of trans-spliced transcripts for chætognath (a) S. cephaloptera and (b) nematode C. elegans. The presence of a SL sequence is related to coding properties and homologous matches in SwissProt (score >150) of the sequences. C. elegans exhibits less non-coding transcripts than S. cephaloptera.

Mentions:
Within the EST collection, 2,914 sequences exhibit SL addition, which represents 30% of nuclear transcripts (Figure 8a). Among the SL population, 72% are coding transcripts, of which 46% have a homolog in SwissProt. The clustering of similar coding trans-spliced transcripts indicated that 41% of putative genes undergo SL addition. Furthermore, the relationship between trans-splicing and expression level was tested through the comparison of the number of ESTs per cluster of trans-spliced or non-trans-spliced transcripts. If we posit that this number can be considered as an estimate of the expression level, trans-spliced genes are significantly more expressed than others (Wilcoxon rank test, p < 2.2e-16). For instance, among the 50 more expressed genes (that is, biggest EST clusters), only two are not trans-spliced. These values suggest that trans-splicing is involved in the regulation of a set of strongly expressed genes responsible for key cellular functions, for example, the RP set.

Figure 8: Categories of trans-spliced transcripts for chætognath (a) S. cephaloptera and (b) nematode C. elegans. The presence of a SL sequence is related to coding properties and homologous matches in SwissProt (score >150) of the sequences. C. elegans exhibits less non-coding transcripts than S. cephaloptera.

Mentions:
Within the EST collection, 2,914 sequences exhibit SL addition, which represents 30% of nuclear transcripts (Figure 8a). Among the SL population, 72% are coding transcripts, of which 46% have a homolog in SwissProt. The clustering of similar coding trans-spliced transcripts indicated that 41% of putative genes undergo SL addition. Furthermore, the relationship between trans-splicing and expression level was tested through the comparison of the number of ESTs per cluster of trans-spliced or non-trans-spliced transcripts. If we posit that this number can be considered as an estimate of the expression level, trans-spliced genes are significantly more expressed than others (Wilcoxon rank test, p < 2.2e-16). For instance, among the 50 more expressed genes (that is, biggest EST clusters), only two are not trans-spliced. These values suggest that trans-splicing is involved in the regulation of a set of strongly expressed genes responsible for key cellular functions, for example, the RP set.

Bottom Line:
Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history.These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.

Background: The chaetognaths (arrow worms) have puzzled zoologists for years because of their astonishing morphological and developmental characteristics. Despite their deuterostome-like development, phylogenomic studies recently positioned the chaetognath phylum in protostomes, most likely in an early branching. This key phylogenetic position and the peculiar characteristics of chaetognaths prompted further investigation of their genomic features.

Results: Transcriptomic and genomic data were collected from the chaetognath Spadella cephaloptera through the sequencing of expressed sequence tags and genomic bacterial artificial chromosome clones. Transcript comparisons at various taxonomic scales emphasized the conservation of a core gene set and phylogenomic analysis confirmed the basal position of chaetognaths among protostomes. A detailed survey of transcript diversity and individual genotyping revealed a past genome duplication event in the chaetognath lineage, which was, surprisingly, followed by a high retention rate of duplicated genes. Moreover, striking genetic heterogeneity was detected within the sampled population at the nuclear and mitochondrial levels but cannot be explained by cryptic speciation. Finally, we found evidence for trans-splicing maturation of transcripts through splice-leader addition in the chaetognath phylum and we further report that this processing is associated with operonic transcription.

Conclusion: These findings reveal both shared ancestral and unique derived characteristics of the chaetognath genome, which suggests that this genome is likely the product of a very original evolutionary history. These features promote chaetognaths as a pivotal model for comparative genomics, which could provide new clues for the investigation of the evolution of animal genomes.